Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment
Multidrug-resistant plasmid-carrying bacteria are of particular clinical concern as they could transfer antibiotic resistance genes to other bacterial species. However, little is known whether evolutionary adaptation of plasmid-carrying bacteria after long-term antibiotic exposure could affect their...
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| Veröffentlicht in: | The ISME Journal 2022-05, Vol.16 (5), p.1284-1293 |
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| creator | Zhang, Peng Mao, Daqing Gao, Huihui Zheng, Liyang Chen, Zeyou Gao, Yuting Duan, Yitao Guo, Jianhua Luo, Yi Ren, Hongqiang |
| description | Multidrug-resistant plasmid-carrying bacteria are of particular clinical concern as they could transfer antibiotic resistance genes to other bacterial species. However, little is known whether evolutionary adaptation of plasmid-carrying bacteria after long-term antibiotic exposure could affect their subsequent colonization of the human gut. Herein, we combined a long-term evolutionary model based on
Escherichia coli
K-12 MG1655 and the multidrug-resistant plasmid RP4 with in vivo colonization experiments in mice. We found that the evolutionary adaptation of plasmid-carrying bacteria to antibiotic exposure facilitated colonization of the murine gut and subsequent plasmid transfer to gut bacteria. The evolved plasmid-carrying bacteria exhibited phenotypic alterations, including multidrug resistance, enhanced bacterial growth and biofilm formation capability and decreased plasmid fitness cost, which might be jointly caused by chromosomal mutations (SNPs in
rpoC
,
proQ
, and
hcaT
) and transcriptional modifications. The upregulated transcriptional genes, e.g., type 1 fimbrial-protein pilus (
fimA
and
fimH
) and the surface adhesin gene (
flu
) were likely responsible for the enhanced biofilm-forming capacity. The gene
tnaA
that encodes a tryptophanase-catalyzing indole formation was transcriptionally upregulated, and increased indole products participated in facilitating the maximum population density of the evolved strains. Furthermore, several chromosomal genes encoding efflux pumps (acriflavine resistance proteins A and B (
acrA, acrB
), outer-membrane protein (
tolC
), multidrug-resistance protein (
mdtM
), and macrolide export proteins A and B (
macA
,
macB
)) were transcriptionally upregulated, while most plasmid-harboring genes (conjugal transfer protein (
traF
) and (
trbB
), replication protein gene (
trfA
), beta-lactamase TEM precursor (
bla
TEM
), aminoglycoside 3'-phosphotransferase (
aphA
) and tetracycline resistance protein A (
tetA
)) were downregulated. Collectively, these findings demonstrated that evolutionary adaptation of plasmid-carrying bacteria in an antibiotic-influenced environment facilitated colonization of the murine gut by the bacteria and plasmids. |
| doi_str_mv | 10.1038/s41396-021-01171-x |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9038720</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2610081494</sourcerecordid><originalsourceid>FETCH-LOGICAL-c474t-8bf07de2fcba04bce173d47c45822efcac867c6c048242589d74c9057231d8b43</originalsourceid><addsrcrecordid>eNp9kUFP3DAQhS1UBJT2D3BAlnrpJWA7TpxckKoVLUgr9dKerYnjLEaJvdgO2q3Ef8dplgV66MmW5s03b-YhdEbJBSV5dRk4zesyI4xmhFJBs80BOqGioJnIBfmw_5fsGH0M4Z6QQpSlOELHOa8TgNcn6GnhemfNH4jGWew6vBojHozyrjEuAm62eN1DGEybKfB-a-wKN6Ci9gawCbgDZXoTIep20upH148TCvwWQwvrOIOjw2CjmZhG4eg1xEHb-AkddtAH_Xn3nqLf369_LW6y5c8ft4tvy0xxwWNWNR0RrWadaoDwRmkq8pYLxYuKMd0pUFUpVKkIrxhnRVW3gqs6bcty2lYNz0_R1cxdj82gW5VGe-jl2pshGZUOjHxfseZOrtyjnM4kGEmArzuAdw-jDlEOJijd92C1G4NkJSWkoryeZn35R3rvRm_TeklV8LoQyX1SsVmVLh2C193eDCVySlfO6cqUrvybrtykpvO3a-xbXuJMgnwWhFSyK-1fZ_8H-wx1ubSK</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2654957173</pqid></control><display><type>article</type><title>Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment</title><source>Oxford Journals Open Access Collection</source><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Zhang, Peng ; Mao, Daqing ; Gao, Huihui ; Zheng, Liyang ; Chen, Zeyou ; Gao, Yuting ; Duan, Yitao ; Guo, Jianhua ; Luo, Yi ; Ren, Hongqiang</creator><creatorcontrib>Zhang, Peng ; Mao, Daqing ; Gao, Huihui ; Zheng, Liyang ; Chen, Zeyou ; Gao, Yuting ; Duan, Yitao ; Guo, Jianhua ; Luo, Yi ; Ren, Hongqiang</creatorcontrib><description>Multidrug-resistant plasmid-carrying bacteria are of particular clinical concern as they could transfer antibiotic resistance genes to other bacterial species. However, little is known whether evolutionary adaptation of plasmid-carrying bacteria after long-term antibiotic exposure could affect their subsequent colonization of the human gut. Herein, we combined a long-term evolutionary model based on
Escherichia coli
K-12 MG1655 and the multidrug-resistant plasmid RP4 with in vivo colonization experiments in mice. We found that the evolutionary adaptation of plasmid-carrying bacteria to antibiotic exposure facilitated colonization of the murine gut and subsequent plasmid transfer to gut bacteria. The evolved plasmid-carrying bacteria exhibited phenotypic alterations, including multidrug resistance, enhanced bacterial growth and biofilm formation capability and decreased plasmid fitness cost, which might be jointly caused by chromosomal mutations (SNPs in
rpoC
,
proQ
, and
hcaT
) and transcriptional modifications. The upregulated transcriptional genes, e.g., type 1 fimbrial-protein pilus (
fimA
and
fimH
) and the surface adhesin gene (
flu
) were likely responsible for the enhanced biofilm-forming capacity. The gene
tnaA
that encodes a tryptophanase-catalyzing indole formation was transcriptionally upregulated, and increased indole products participated in facilitating the maximum population density of the evolved strains. Furthermore, several chromosomal genes encoding efflux pumps (acriflavine resistance proteins A and B (
acrA, acrB
), outer-membrane protein (
tolC
), multidrug-resistance protein (
mdtM
), and macrolide export proteins A and B (
macA
,
macB
)) were transcriptionally upregulated, while most plasmid-harboring genes (conjugal transfer protein (
traF
) and (
trbB
), replication protein gene (
trfA
), beta-lactamase TEM precursor (
bla
TEM
), aminoglycoside 3'-phosphotransferase (
aphA
) and tetracycline resistance protein A (
tetA
)) were downregulated. Collectively, these findings demonstrated that evolutionary adaptation of plasmid-carrying bacteria in an antibiotic-influenced environment facilitated colonization of the murine gut by the bacteria and plasmids.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-021-01171-x</identifier><identifier>PMID: 34903849</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/23 ; 42/44 ; 45/29 ; 45/43 ; 45/77 ; 45/91 ; 631/181/735 ; 631/326/22/1290 ; 64/60 ; Acriflavine ; Adaptation ; Aminoglycoside antibiotics ; Aminoglycosides ; Animals ; Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Bacteria ; Biofilms ; Biomedical and Life Sciences ; Colonization ; Drug resistance ; Drug Resistance, Multiple, Bacterial ; E coli ; Ecological adaptation ; Ecology ; Efflux ; Escherichia coli - genetics ; Escherichia coli K12 - genetics ; Escherichia coli Proteins - genetics ; Evolution ; Evolutionary Biology ; Gastrointestinal Microbiome ; Genes ; Indoles ; Intestinal microflora ; Life Sciences ; Membrane proteins ; Mice ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microbiota ; Multidrug resistance ; Multidrug Resistance-Associated Proteins - genetics ; Mutation ; Phosphotransferase ; Plasmids ; Plasmids - genetics ; Population density ; Protein A ; Protein transport ; Proteins ; RNA-Binding Proteins - genetics ; Single-nucleotide polymorphism ; Transcription ; Tryptophan 2,3-dioxygenase ; β Lactamase</subject><ispartof>The ISME Journal, 2022-05, Vol.16 (5), p.1284-1293</ispartof><rights>The Author(s) 2021</rights><rights>2021. The Author(s).</rights><rights>The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-8bf07de2fcba04bce173d47c45822efcac867c6c048242589d74c9057231d8b43</citedby><cites>FETCH-LOGICAL-c474t-8bf07de2fcba04bce173d47c45822efcac867c6c048242589d74c9057231d8b43</cites><orcidid>0000-0002-3109-2767 ; 0000-0003-0313-0129 ; 0000-0001-7707-708X ; 0000-0002-1371-9917 ; 0000-0002-7943-0657 ; 0000-0002-4732-9175</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9038720/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9038720/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34903849$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Peng</creatorcontrib><creatorcontrib>Mao, Daqing</creatorcontrib><creatorcontrib>Gao, Huihui</creatorcontrib><creatorcontrib>Zheng, Liyang</creatorcontrib><creatorcontrib>Chen, Zeyou</creatorcontrib><creatorcontrib>Gao, Yuting</creatorcontrib><creatorcontrib>Duan, Yitao</creatorcontrib><creatorcontrib>Guo, Jianhua</creatorcontrib><creatorcontrib>Luo, Yi</creatorcontrib><creatorcontrib>Ren, Hongqiang</creatorcontrib><title>Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Multidrug-resistant plasmid-carrying bacteria are of particular clinical concern as they could transfer antibiotic resistance genes to other bacterial species. However, little is known whether evolutionary adaptation of plasmid-carrying bacteria after long-term antibiotic exposure could affect their subsequent colonization of the human gut. Herein, we combined a long-term evolutionary model based on
Escherichia coli
K-12 MG1655 and the multidrug-resistant plasmid RP4 with in vivo colonization experiments in mice. We found that the evolutionary adaptation of plasmid-carrying bacteria to antibiotic exposure facilitated colonization of the murine gut and subsequent plasmid transfer to gut bacteria. The evolved plasmid-carrying bacteria exhibited phenotypic alterations, including multidrug resistance, enhanced bacterial growth and biofilm formation capability and decreased plasmid fitness cost, which might be jointly caused by chromosomal mutations (SNPs in
rpoC
,
proQ
, and
hcaT
) and transcriptional modifications. The upregulated transcriptional genes, e.g., type 1 fimbrial-protein pilus (
fimA
and
fimH
) and the surface adhesin gene (
flu
) were likely responsible for the enhanced biofilm-forming capacity. The gene
tnaA
that encodes a tryptophanase-catalyzing indole formation was transcriptionally upregulated, and increased indole products participated in facilitating the maximum population density of the evolved strains. Furthermore, several chromosomal genes encoding efflux pumps (acriflavine resistance proteins A and B (
acrA, acrB
), outer-membrane protein (
tolC
), multidrug-resistance protein (
mdtM
), and macrolide export proteins A and B (
macA
,
macB
)) were transcriptionally upregulated, while most plasmid-harboring genes (conjugal transfer protein (
traF
) and (
trbB
), replication protein gene (
trfA
), beta-lactamase TEM precursor (
bla
TEM
), aminoglycoside 3'-phosphotransferase (
aphA
) and tetracycline resistance protein A (
tetA
)) were downregulated. Collectively, these findings demonstrated that evolutionary adaptation of plasmid-carrying bacteria in an antibiotic-influenced environment facilitated colonization of the murine gut by the bacteria and plasmids.</description><subject>38/23</subject><subject>42/44</subject><subject>45/29</subject><subject>45/43</subject><subject>45/77</subject><subject>45/91</subject><subject>631/181/735</subject><subject>631/326/22/1290</subject><subject>64/60</subject><subject>Acriflavine</subject><subject>Adaptation</subject><subject>Aminoglycoside antibiotics</subject><subject>Aminoglycosides</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Biofilms</subject><subject>Biomedical and Life Sciences</subject><subject>Colonization</subject><subject>Drug resistance</subject><subject>Drug Resistance, Multiple, Bacterial</subject><subject>E coli</subject><subject>Ecological adaptation</subject><subject>Ecology</subject><subject>Efflux</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli K12 - genetics</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Evolution</subject><subject>Evolutionary Biology</subject><subject>Gastrointestinal Microbiome</subject><subject>Genes</subject><subject>Indoles</subject><subject>Intestinal microflora</subject><subject>Life Sciences</subject><subject>Membrane proteins</subject><subject>Mice</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microbiota</subject><subject>Multidrug resistance</subject><subject>Multidrug Resistance-Associated Proteins - genetics</subject><subject>Mutation</subject><subject>Phosphotransferase</subject><subject>Plasmids</subject><subject>Plasmids - genetics</subject><subject>Population density</subject><subject>Protein A</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>RNA-Binding Proteins - genetics</subject><subject>Single-nucleotide polymorphism</subject><subject>Transcription</subject><subject>Tryptophan 2,3-dioxygenase</subject><subject>β Lactamase</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kUFP3DAQhS1UBJT2D3BAlnrpJWA7TpxckKoVLUgr9dKerYnjLEaJvdgO2q3Ef8dplgV66MmW5s03b-YhdEbJBSV5dRk4zesyI4xmhFJBs80BOqGioJnIBfmw_5fsGH0M4Z6QQpSlOELHOa8TgNcn6GnhemfNH4jGWew6vBojHozyrjEuAm62eN1DGEybKfB-a-wKN6Ci9gawCbgDZXoTIep20upH148TCvwWQwvrOIOjw2CjmZhG4eg1xEHb-AkddtAH_Xn3nqLf369_LW6y5c8ft4tvy0xxwWNWNR0RrWadaoDwRmkq8pYLxYuKMd0pUFUpVKkIrxhnRVW3gqs6bcty2lYNz0_R1cxdj82gW5VGe-jl2pshGZUOjHxfseZOrtyjnM4kGEmArzuAdw-jDlEOJijd92C1G4NkJSWkoryeZn35R3rvRm_TeklV8LoQyX1SsVmVLh2C193eDCVySlfO6cqUrvybrtykpvO3a-xbXuJMgnwWhFSyK-1fZ_8H-wx1ubSK</recordid><startdate>20220501</startdate><enddate>20220501</enddate><creator>Zhang, Peng</creator><creator>Mao, Daqing</creator><creator>Gao, Huihui</creator><creator>Zheng, Liyang</creator><creator>Chen, Zeyou</creator><creator>Gao, Yuting</creator><creator>Duan, Yitao</creator><creator>Guo, Jianhua</creator><creator>Luo, Yi</creator><creator>Ren, Hongqiang</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3109-2767</orcidid><orcidid>https://orcid.org/0000-0003-0313-0129</orcidid><orcidid>https://orcid.org/0000-0001-7707-708X</orcidid><orcidid>https://orcid.org/0000-0002-1371-9917</orcidid><orcidid>https://orcid.org/0000-0002-7943-0657</orcidid><orcidid>https://orcid.org/0000-0002-4732-9175</orcidid></search><sort><creationdate>20220501</creationdate><title>Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment</title><author>Zhang, Peng ; Mao, Daqing ; Gao, Huihui ; Zheng, Liyang ; Chen, Zeyou ; Gao, Yuting ; Duan, Yitao ; Guo, Jianhua ; Luo, Yi ; Ren, Hongqiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-8bf07de2fcba04bce173d47c45822efcac867c6c048242589d74c9057231d8b43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>38/23</topic><topic>42/44</topic><topic>45/29</topic><topic>45/43</topic><topic>45/77</topic><topic>45/91</topic><topic>631/181/735</topic><topic>631/326/22/1290</topic><topic>64/60</topic><topic>Acriflavine</topic><topic>Adaptation</topic><topic>Aminoglycoside antibiotics</topic><topic>Aminoglycosides</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Biofilms</topic><topic>Biomedical and Life Sciences</topic><topic>Colonization</topic><topic>Drug resistance</topic><topic>Drug Resistance, Multiple, Bacterial</topic><topic>E coli</topic><topic>Ecological adaptation</topic><topic>Ecology</topic><topic>Efflux</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli K12 - genetics</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Evolution</topic><topic>Evolutionary Biology</topic><topic>Gastrointestinal Microbiome</topic><topic>Genes</topic><topic>Indoles</topic><topic>Intestinal microflora</topic><topic>Life Sciences</topic><topic>Membrane proteins</topic><topic>Mice</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Microbiota</topic><topic>Multidrug resistance</topic><topic>Multidrug Resistance-Associated Proteins - genetics</topic><topic>Mutation</topic><topic>Phosphotransferase</topic><topic>Plasmids</topic><topic>Plasmids - genetics</topic><topic>Population density</topic><topic>Protein A</topic><topic>Protein transport</topic><topic>Proteins</topic><topic>RNA-Binding Proteins - genetics</topic><topic>Single-nucleotide polymorphism</topic><topic>Transcription</topic><topic>Tryptophan 2,3-dioxygenase</topic><topic>β Lactamase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Peng</creatorcontrib><creatorcontrib>Mao, Daqing</creatorcontrib><creatorcontrib>Gao, Huihui</creatorcontrib><creatorcontrib>Zheng, Liyang</creatorcontrib><creatorcontrib>Chen, Zeyou</creatorcontrib><creatorcontrib>Gao, Yuting</creatorcontrib><creatorcontrib>Duan, Yitao</creatorcontrib><creatorcontrib>Guo, Jianhua</creatorcontrib><creatorcontrib>Luo, Yi</creatorcontrib><creatorcontrib>Ren, Hongqiang</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Peng</au><au>Mao, Daqing</au><au>Gao, Huihui</au><au>Zheng, Liyang</au><au>Chen, Zeyou</au><au>Gao, Yuting</au><au>Duan, Yitao</au><au>Guo, Jianhua</au><au>Luo, Yi</au><au>Ren, Hongqiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2022-05-01</date><risdate>2022</risdate><volume>16</volume><issue>5</issue><spage>1284</spage><epage>1293</epage><pages>1284-1293</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Multidrug-resistant plasmid-carrying bacteria are of particular clinical concern as they could transfer antibiotic resistance genes to other bacterial species. However, little is known whether evolutionary adaptation of plasmid-carrying bacteria after long-term antibiotic exposure could affect their subsequent colonization of the human gut. Herein, we combined a long-term evolutionary model based on
Escherichia coli
K-12 MG1655 and the multidrug-resistant plasmid RP4 with in vivo colonization experiments in mice. We found that the evolutionary adaptation of plasmid-carrying bacteria to antibiotic exposure facilitated colonization of the murine gut and subsequent plasmid transfer to gut bacteria. The evolved plasmid-carrying bacteria exhibited phenotypic alterations, including multidrug resistance, enhanced bacterial growth and biofilm formation capability and decreased plasmid fitness cost, which might be jointly caused by chromosomal mutations (SNPs in
rpoC
,
proQ
, and
hcaT
) and transcriptional modifications. The upregulated transcriptional genes, e.g., type 1 fimbrial-protein pilus (
fimA
and
fimH
) and the surface adhesin gene (
flu
) were likely responsible for the enhanced biofilm-forming capacity. The gene
tnaA
that encodes a tryptophanase-catalyzing indole formation was transcriptionally upregulated, and increased indole products participated in facilitating the maximum population density of the evolved strains. Furthermore, several chromosomal genes encoding efflux pumps (acriflavine resistance proteins A and B (
acrA, acrB
), outer-membrane protein (
tolC
), multidrug-resistance protein (
mdtM
), and macrolide export proteins A and B (
macA
,
macB
)) were transcriptionally upregulated, while most plasmid-harboring genes (conjugal transfer protein (
traF
) and (
trbB
), replication protein gene (
trfA
), beta-lactamase TEM precursor (
bla
TEM
), aminoglycoside 3'-phosphotransferase (
aphA
) and tetracycline resistance protein A (
tetA
)) were downregulated. Collectively, these findings demonstrated that evolutionary adaptation of plasmid-carrying bacteria in an antibiotic-influenced environment facilitated colonization of the murine gut by the bacteria and plasmids.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>34903849</pmid><doi>10.1038/s41396-021-01171-x</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-3109-2767</orcidid><orcidid>https://orcid.org/0000-0003-0313-0129</orcidid><orcidid>https://orcid.org/0000-0001-7707-708X</orcidid><orcidid>https://orcid.org/0000-0002-1371-9917</orcidid><orcidid>https://orcid.org/0000-0002-7943-0657</orcidid><orcidid>https://orcid.org/0000-0002-4732-9175</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1751-7362 |
| ispartof | The ISME Journal, 2022-05, Vol.16 (5), p.1284-1293 |
| issn | 1751-7362 1751-7370 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9038720 |
| source | Oxford Journals Open Access Collection; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | 38/23 42/44 45/29 45/43 45/77 45/91 631/181/735 631/326/22/1290 64/60 Acriflavine Adaptation Aminoglycoside antibiotics Aminoglycosides Animals Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Bacteria Biofilms Biomedical and Life Sciences Colonization Drug resistance Drug Resistance, Multiple, Bacterial E coli Ecological adaptation Ecology Efflux Escherichia coli - genetics Escherichia coli K12 - genetics Escherichia coli Proteins - genetics Evolution Evolutionary Biology Gastrointestinal Microbiome Genes Indoles Intestinal microflora Life Sciences Membrane proteins Mice Microbial Ecology Microbial Genetics and Genomics Microbiology Microbiota Multidrug resistance Multidrug Resistance-Associated Proteins - genetics Mutation Phosphotransferase Plasmids Plasmids - genetics Population density Protein A Protein transport Proteins RNA-Binding Proteins - genetics Single-nucleotide polymorphism Transcription Tryptophan 2,3-dioxygenase β Lactamase |
| title | Colonization of gut microbiota by plasmid-carrying bacteria is facilitated by evolutionary adaptation to antibiotic treatment |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-07T21%3A03%3A10IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Colonization%20of%20gut%20microbiota%20by%20plasmid-carrying%20bacteria%20is%20facilitated%20by%20evolutionary%20adaptation%20to%20antibiotic%20treatment&rft.jtitle=The%20ISME%20Journal&rft.au=Zhang,%20Peng&rft.date=2022-05-01&rft.volume=16&rft.issue=5&rft.spage=1284&rft.epage=1293&rft.pages=1284-1293&rft.issn=1751-7362&rft.eissn=1751-7370&rft_id=info:doi/10.1038/s41396-021-01171-x&rft_dat=%3Cproquest_pubme%3E2610081494%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2654957173&rft_id=info:pmid/34903849&rfr_iscdi=true |